J. exp. Biol. 141, 447-451 (1989)
Printed in Great Britain © The Company of Biologists Limited 1989
447
SHORT COMMUNICATION
ATTACHED MAGNETS IMPAIR MAGNETIC FIELD
DISCRIMINATION BY HONEYBEES
BY MICHAEL M. WALKER AND M. E. BITTERMAN
Btkisy Laboratory of Neurobiology, University of Hawaii,
1993 East-West Road, Honolulu, HI 96822, USA
Accepted 13 July 1988
Evidence that honeybees respond to magnetic fields comes from both orientation (Lindauer & Martin, 1968, 1972; Towne & Gould, 1985) and conditioning
experiments (Walker & Bitterman, 1985; Walker et al. 1988a). Perhaps because
suitable behavioural methods have not yet been developed, the effects obtained
are not very large. They are, however, reliable enough to permit evaluation of the
ferromagnetic transduction hypothesis (Ising, 1945; Lowenstam, 1962; Gould et al.
1978; Kirschvink & Walker, 1985), to which the discovery of large numbers of
single-domain particles of magnetite in the anterodorsal abdominal region of
honeybees lends credence (Gould et al. 1978), and which alone among the various
transduction hypotheses that have been proposed (Kirschvink & Gould, 1981;
Kirschvink & Walker, 1985; Yorke, 1981; Kalmijn, 1974; Jungerman & Rosenblum, 1980; Leask, 1977; Korall & Martin, 1987) predicts that discrimination can
be abolished by magnets attached in the vicinity of those particles (Jungerman &
Rosenblum, 1980; Kirschvink & Walker, 1985). Free-flying honeybees were
trained in two experiments to discriminate a local anomaly in the ambient
magnetic field. Animals carrying small pieces of magnetized steel wire glued to the
anterodorsal abdomen failed in the task, but untreated animals and control
animals carrying small pieces of nonmagnetic wire succeeded. The results imply
that the magnetite crystals in the anterodorsal abdomen play a critical role in
magnetoreception by honeybees.
Individual foragers from our own hives were trained to shuttle back and forth
between the hives and a small wooden shed adjacent to the laboratory. Set 14 cm
apart on a table in the shed were two identical targets, 5 cm in diameter, each
containing a food well so constructed that a shock could be delivered when the
proboscis made contact with liquid in the well (Abramson, 1986). Directly beneath
the table and centred on the targets were two pairs of coils, each pair consisting of
an inner (4 cm diameter, 50 turns) and an outer (10 cm diameter, 8 turns) coil. One
of the pairs (the left on some visits and the right on others, in balanced
quasirandom order) was energized to produce a localized, vertically oriented
magnetic dipole anomaly with a radius of 5 cm and a peak intensity of 350 microKey words: honeybees, Apis mellifera, magnetite, magnetoreception.
448
M . M . W A L K E R AND M. E. BITTERMAN
Tesla (/iT; field measured with a Develco 9200C model three-axis fluxgate
magnetometer). The anomaly was superimposed on the uniform background
Hawaiian field (total intensity 38 f/T, inclination 38°, declination 11°16'E). The
well of the target in the ambient field (designated S—) contained an unacceptable
saline solution, contacts with which were punished with shock on all visits after the
first on which an error was made. (The shock was set initially at 2 V and increased
in 1V steps to 4 V with each successive initial error.) The well of the target in the
anomalous field (S+) contained 50% sucrose solution which the animal drank to
repletion on each visit (whether upon correct initial choice or after some
experience with S - ) . An observer recorded the initial choice made on each visit.
In experiment 1, three groups of bees were trained for 16 visits. There was a
magnetic group of eight subjects, each carrying a 1-2 mm length of magnetized
stainless-steel wire glued to the anterodorsal surface of the abdomen; a control
group of eight subjects carrying nonmagnetic pieces of copper wire instead; and an
untreated group of eight subjects. The pieces of stainless-steel wire (0-36 mm
diameter) were magnetized by a unidirectional magnetic field pulse with a peak
intensity of 100 mT. Copper wires of the same length and gauge were attached to
control animals. The subjects were chosen at random from groups of foragers at a
feeding station providing 10-12% sucrose solution and were anaesthetized by
chilling for wire attachment. The wings of the immobilized animal were held apart
with padded nonmetallic forceps and the wire attached with rubber cement in the
dorsal midline as close to the front of the abdomen as possible, a location chosen
on the basis of the study of Gould et al. (1978) and further information provided by
J. L. Kirschvink. The animal was then marked with coloured lacquer, returned to
the feeder where it was fed some 50 % sucrose solution, and permitted to resume
normal foraging for at least 1 day before testing. Tagged subjects were found at the
feeder up to 9 days after the treatment. The attached steel or copper wires could
be distinguished easily by their colour in experiment 1.
As Table 1 shows, the performance even of the untreated group in experiment 1
was not spectacularly good - the mean proportion of correct choices in the 16 visits
was only about 0-66 - but there was clear evidence of discrimination. Every
untreated animal made more than eight correct choices (P = 0-0039), and the same
was true of the control animals, but the performance of only four of the magnetic
animals exceeded the chance expectation (P>0-05). The median test showed the
performance of the control animals to be significantly better than that of the
Table 1. Mean proportion of correct choices and its standard error (S.E.) for each
group in each experiment
Experiment 1
N
Mean
S.E.
N
Mean
S.E.
Untreated
Control
Magnetic
0-66
0-63
0-58
0-02
003
0-04
8
16
10
0-68
0-63
0-55
002
002
002
OO OO
Group
00
Experiment 2
Magnetic field discrimination by honeybees
449
magnetic animals (P = 0-0385), with no significant difference between the
untreated animals and the controls (P>0-05).
Experiment 2 differed from the first experiment in only one important respect:
the observer did not know which were magnetic and which were control animals
until the conclusion of the experiment, because the wires attached to the magnetic
and control animals had been made indistinguishable from each other with a
coating of coloured lacquer. It was found after the experiment that 10 magnetic
animals and 16 control animals had completed the 16 scheduled training visits.
Each piece of wire to be used was assigned to a bee according to a randomized key
in the possession of a member of our laboratory not involved in the work. Each
bee was given an identification number and marked uniquely with spots of
coloured lacquer to permit decoding of the data when the experiment was
finished. Of 80 wires prepared, 78 were attached to animals successfully. Of these
tagged animals, we attempted to train 44 subsequently found at the feeder.
As Table 1 shows, the results of the second experiment were very much the
same as those of the first. All eight untreated animals (P = 0-0039) and 13 of the 16
control animals (P = 0-0105), but only four of the 10 magnetic animals (P > 0-05),
made more than eight correct choices in the 16 visits. The median test again
showed significantly better performance in the control animals than in the
magnetic animals (P = 0-0208), with no significant difference between the
untreated animals and the controls (P>0-05). The differential effectiveness of
the two treatments is indicated by another measure; the number of animals whose
training was begun but that did not return for the prescribed number of training
visits. The number of such animals increases when shock for error is used in an
effort to sharpen performance in a difficult discrimination task and may in fact be
taken as an index of the difficulty of the task. Of 21 animals selected at random
that turned out to be carrying copper wire, only five failed to return for 16 visits, as
compared with 13 of 23 animals carrying magnetic wire (P = 0-0279).
These results are not only consistent with the ferromagnetic transduction
hypothesis but imply strongly that the magnetite crystals found in the anterodorsal
abdomen play a critical role. The results of dance experiments with honeybees
(Lindauer & Martin, 1968) suggest that the magnetoreceptor system is disabled in
fields of greater intensity than 500 ^T, such as are found within 1-2 mm of the
magnetized wires we used (Walker et al. 19886). Because the field decays rapidly
to 10 jxT (20% of earth-strength) at a distance of 5 mm from the wires, it seems
reasonable to conclude that the magnetoreceptors must have been very near the
wires, whose position was dictated by the locus of the magnetite. It should be
noted that there is precedent for our work. Magnetic attachments to the heads of
pigeons, which also contain magnetite (Walcott et al. 1979), have been found to
impair homing (Keeton, 1972), although not to prevent it entirely, perhaps
because other cues were available (Walraff, 1983). Experiments like ours, in which
better-than-chance performance is possible only on the basis of magnetic-field
stimuli, must await evidence of conditioned response to magnetic fields, which has
been difficult to demonstrate in pigeons (Ossenkopp & Barbeito, 1978).
450
M . M . W A L K E R AND M. E . BITTERMAN
Magnetite particles useful for magnetoreception can be recognized easily when
they are concentrated in small volumes of tissue (Kirschvink, 1983; Walker et al.
1985). Such concentrations have been found in widely divergent animals (Walker
et al. 1984, 1988a,6; Kirschvink et al. 1985), of which tuna (Walker, 1984) and
salmon (Quinn, 1980) as well as pigeons and honeybees are known to respond to
magnetic-field stimuli. It follows from the hypothesis of magnetite-based magnetoreception, which is supported by our results, that magnetosensory capabilities
may exist in species for which there is as yet no behavioural evidence of any
magnetic sensitivity.
This project was supported by grant BNS-8519425 from the National Science
Foundation. We thank J. L. Kirschvink of the California Institute of Technology
for supplying the steel wire, for the loan of the impulse magnetization unit to
magnetize the steel wire, for advice on coil design, and for helpful discussions. For
assistance in the collection of these data, we thank Mei Yee Wong.
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